Introduction

Brazil has the largest commercial herd in the world, with 208 million animals. It is also the largest beef exporter, the second largest meat producer and the fifth milk producer (34.5 million tons) (USDA 2014). According to the Brazilian cattle headcount, around 28.24 million are located in the Northeast region, a high number when compared to the goat and sheep headcount in the region, 7.84 and 9.32 million, respectively (IBGE 2012). It is clear that the main livestock activity in the Northeast region is cattle production, which has a great socioeconomic importance in the region.

In beef cattle activity, it is common using grains and cereals in animal diet by producers. Among them, corn is the most used as an energy ingredient. However, in the Northeast region, there is no significant production of these ingredients. They must be purchased from other regions, making the activity expensive. Prosopis juliflora (SW) D.C., known in Northeastern Brazil as mesquite or mesquite tree, is a plant that stands out in the semiarid region. It is well adapted to the conditions of the region, bearing fruits during the dry season. Its fruits (pods) have a high nutritional value.

The nutritional value of mesquite is concentrated in the pods, which are an excellent energy source. They are compared to the energy value of corn (Alves et al., 2010). Cattle can consume in natura mesquite pods when they are loose in the pasture. However, this is not recommended, as besides being able to cause perforations in the gastrointestinal tract, there may be active alkaloid principle intoxication, causing the masseter muscle to stiffen because it affects cattle central nervous system. Therefore, pod meal manufacturing is the most appropriate way to use mesquite pods in cattle feed because pods undergo a heat process (60–80 °C) when collected and are subsequently ground, neutralizing the anti-nutritional factors in the pods. Argôlo et al. (2010) reported that the quantity of microbial nitrogen synthesis and efficiency of microbial protein synthesis, organic matter intake, and non-fiber carbohydrates intake presented a linear negative response to the replacement of corn by mesquite pod meal of the diet of lactating goats.

The objectives of this study was to evaluate the effects corn total replacement for mesquite pod meal on nutritional value, performance, feeding behavior, nitrogen balance, and microbial protein synthesis of Holstein-Zebu crossbred dairy steers diet.

Materials and methods

Site, period, facilities, and animals

The experiment was conducted at the Academic Unit of Serra Talhada, which belongs to the Federal Rural University of Pernambuco, state of Pernambuco, Northeastern Brazil, between May and September 2013. The experiment lasted 84 days, divided into three periods of 28 days. The region has an irregular rainfall, with a 700-mm annual average, of which 108 mm occurs between May and September. In addition, the thermal regime is characterized by high temperatures, with a maximum value of 31 °C (INMET 2013).

Animals were kept in individual stalls (3 × 9 m) surrounded by a smooth wire with fibre-cement tile floors. Each stall had a feeder (1.0 m long). The water dispenser was replaced by a waterer. The study included 25 crossbred Holstein-Zebu bulls, with an initial body weight of 219 ± 22 kg and a mean age of 18 months. They were purchased from a commercial herd. Initially, the animals were weighed, identified, and treated against endo and ectoparasites.

Experimental diets

Experimental diets were composed of Tifton 85 hay, soybean meal, ground corn, mesquite pod meal, and mineral salt. Diets were formulated according to the recommendations of the NRC (2000) for 1.0 kg/day weight gains. After a period of adaptation (15 days) receiving the same diet, the animals were randomly distributed in treatments containing five levels of replacement of corn by mesquite pod meal: 0, 250, 500, 750, and 1000 g/kg on a dry matter basis (Table 1) as total mixed ration. The mesquite pod meal was purchased from a Company (Reunidas Rio de Contas Farm Ltda. – RIOCON). Feeding was done twice a day at 08:00 and 16:00 h to allow for ad libitum intake and adjusted next feed upward by 5 % leftover every day.

Table 1 Proportion of ingredients, chemical composition of experimental diets and chemical composition of ingredients
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Nutrients intake and digestibility

The dry matter intake was determined by the difference between offered food amounts and leftovers. During the experiment, every morning, before offering the food, leftovers were collected and weighed, and the data were recorded for daily control.

Samples of offered food were collected during the last 3 days of each period (Tifton 85 hay, soybean meal, corn grain, mesquite pod meal, and mineral salt), and leftovers were collected daily, with samples being bulked per week. Samples were pre-dried in a forced ventilation oven at 55 ± 5 °C for 72 h and ground in a Willey cutting mill with 1-mm diameter sieves in order to analyze dry matter (DM) (method 967.03), mineral matter (MM) (method 942.05), organic matter (OM), and crude protein (CP) (method 988.05) contents following the recommendations of the Association of Official Analytical Chemists (AOAC 1990). Neutral detergent fiber (NDF) was analyzed according to Van Soest et al. (1991) using alpha-amylase, as recommended by AOAC (1990). Ether extract (method 920.29) was determined using an ANKOM XT-15 Extractor. The extraction is conducted at a high temperature (90 °C) in a closed system for 60 min using hexane as organic solvent (AOAC 1990). For the estimation of total carbohydrates, non-fiber carbohydrates, and total digestible nutrients, the equations of Sniffen et al. (1992), Hall et al. (2000), and Weiss (1999), respectively, were used.

To estimate the fecal dry matter production, indigestible dry matter (iDM) was used as an internal indicator. Fecal samples, food offered, and leftovers were sieved in a Willey mill with a 2-mm mesh sieve and packed in 4 × 5 cm TNT bags (TNT—100 μ). The samples were placed in bags with 20 mg of dry matter/cm2 (5 g per bag) of surface and incubated in the rumen of fistulated cattle (different from initial group) for 288 h, following the recommendations of Casali et al. (2008).

Performance and feeding behavior evaluation

At the end of each 28-days period, the remaining animals were weighed after fasting of solid food for approximately 16 h to determine total weight gain and average daily gain. Feed efficiency was calculated as the ratio between average daily gain (kg/day) and dry matter intake (kg/day). Behavioral pattern assessments were performed using instantaneous scans in 5-min intervals for three 12-h consecutive days (06:00–18:00). The following activities were observed: feed intake, rumination, mastication, and idleness total time.

Nitrogen balance and microbial protein synthesis

A single urine sample from each animal, named “spot,” was collected on the last day of each collection period approximately 4 h after the first feeding during spontaneous urination. A 10-mL urine sample was immediately diluted into 40 mL of sulfuric acid at 0.036 N, keeping the pH below 3 in order to avoid nitrogen compound decomposition and uric acid precipitation. Samples from each animal kept frozen at −20 °C prior to the analysis. The end-point method was used to estimate creatinine concentration in urine via picrate and acidifier (Doles® commercial kits). In order to obtain daily creatinine excretion, an average of 27.36 mg/kg of body weight (BW) was used. It was obtained by Rennó et al. (2000) for cattle.

In offered food, leftovers, feces, and urine composite samples, the total nitrogen content was determined by the micro Kjeldahl method according to the methodology described by the method 988.05 (AOAC 1990). Microbial protein synthesis was determined by the technique purine derivatives (PD). PD excretion in the urine was calculated by multiplying daily urine volume by the sum of allantoin and uric acid concentration in the daily urine samples. Absorbed purine calculation was assessed from PD excretion by the formula: PD = (0.85 × Pabs) + (0.385 × BW0.75). Microbial nitrogen was calculated from absorbed purines using the formula Nmic = (70 × Pabs)/(0.83 × 0.134 × 1000) (Chen and Gomes 1992).

Experimental design and statistical analysis

The experimental design was completely randomized, with five treatments and five repetitions per treatment. The statistical model used for analyzes was Y ij = μ + T i + ε ij, where Y ij is response variable, μ is global mean, T i is treatment effect, and ε ij is random error. Data were analyzed using PROC GLM for analysis of variance and PROC REG for regression analysis using the software Systems Statistical Analysis version 9.1 (SAS 2009). Data normality (Shapiro-Wilk test at 5 % probability) was verified by the UNIVARIATE procedure (PROC UNIVARIATE) of SAS. Standard error of the mean was obtained from original data. Differences between treatments were considered significant when P < 0.05.

Results

Nutrients intake, animal performance, and feeding behavior

Replacing corn by mesquite pod meal did not significantly affect (P > 0.05) the intake of dry matter, organic matter, neutral detergent fiber, crude protein, total carbohydrates, non-fiber carbohydrates, and total digestible nutrients (Table 2). Significant differences (P > 0.05) were also not observed regarding initial and final body weights, total weight gain, average daily gain, and food conversion (Table 2). Cattle feeding behavior did not change time spent feeding, ruminating, masticating, or on idleness (P > 0.05) between levels of replacement of corn by mesquite pod meal in experimental diets (Table 2).

Table 2 Nutrient intake, performance and feeding behavior of male dairy cattle fed with mesquite pod meal replacing corn
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Digestibility, nitrogen balance, and microbial protein synthesis

The total replacement of corn by mesquite pod meal did not significantly affect (P > 0.05) the digestibility of dry matter, organic matter, crude protein, neutral detergent fiber, non-fiber carbohydrates, total carbohydrate, and total digestible nutrients (Table 3). Nitrogen intake, voided in feces, voided in urine, and digested and retained had no significant differences between levels of replacement of corn by mesquite pod meal (P > 0.05) as well as retained nitrogen: consumed nitrogen ratio had a mean value of 0.63 (Table 3).

Table 3 Nutrients digestibility, nitrogen balance, and microbial protein synthesis in function of levels of replacement of corn by mesquite pod meal
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Microbial protein synthesis and efficiency also showed no statistical difference (P > 0.05) between analyzed replacement levels, with mean values of 443.13 g/day for microbial protein synthesis and 120.32 g/kg of total digestible nutrients (TDN) for microbial synthesis efficiency (Table 3).

Discussion

The similarity of composition of experimental diets (Table 2) favored no limitations on nutrient intake, as the replacement of corn by mesquite pod meal did not limit intake by physical, physiological, and psychogenic effects. Thus, animal maintenance and production requirements were observed, causing a similarity of weight gain regarding the five replacement levels (Table 2). NRC (2000) reported 6.14, 0.820 and 4 kg/day of dry matter, crude protein, and TDN requirement, respectively, for steers with a 220 kg body weight and an average daily gain of 1.0 kg/day. In this study, dry matter, crude protein and TDN intake showed mean values of 6.994, 0.831, and 3.991 kg/day, respectively (Table 2). It is similar to that previously reported by NRC (2000) because the similarity of concentrations of crude protein and energy content favored the similarity of experimental diets, i.e., final body weight, total weight gain, average daily gain, and feed conversion.

In this evaluation, the feeding behavior was not influenced by mesquite pod meal replacing corn. However, data presented by Pereira et al. (2013) stated that the addition of mesquite pod meal in the diet increases the time spent on feeding, ruminating and idleness.

It is noteworthy that the analyzed weight gain rates were very close to those described by the national literature for crossbred European x Zebu and Nellore cattle (Missio et al., 2009; Silva et al., 2012). Thus, it is evident that these dairy cattle have similar performance characteristics to beef cattle. They contribute highly to genetics of Zebu animals, thus favoring a better utilization of fiber because they are more rustic and adapted to Brazilian conditions. Silva et al. (2012) reported that babassu mesocarp bran might partially replace corn in cattle feed, which showed a higher weight gain and feed conversion at 60 % replacement.

Nutrient digestibility was not affected by replacing corn by mesquite pod meal. This can probably be related to the quality of the ingredient under evaluation. Similarity between total carbohydrates and non-fiber carbohydrates contents of the two energy concentrates, corn, and mesquite pod meal (Table 2) favored the best use of these nutrients by rumen microorganisms. Contrary to corn, mesquite pod meal does not have a high starch content in its composition. However, it has a high content of organic acids and sugars, particularly sucrose. This allows for a readily available energy for the microorganisms in synchrony with protein. Furthermore, the diet appears to be acceptable by animals due to palatability (Alves et al., 2010; Santos et al., 2015). However, data that are more recent suggest that the fact that mesquite pods are high on non-fiber carbohydrates content is due to larger proportions of mannose and galactose monosaccharides, 62.52 and 35.92 %, respectively (Rincón et al. 2014). Although corn and mesquite pod meal present differences in the constitution of non-fiber carbohydrates, these differences are not enough to cause changes in the rumen environment and, consequently, in digestibility. Argôlo et al. (2010), working with total replacement of corn by mesquite pod meal, found no significant differences for pH, ammonia and short-chain fatty acid profile.

Mesquite pod meal is an excellent alternative to replace corn. Cardoso et al. (2013), evaluating the partial replacement of corn by alternative energy sources (millet and sorghum grains and soybean hulls) for Nellore cattle, concluded that it is possible to replace up to 50 % levels. Changes in consumption and digestibility of nutrients will thus not occur.

Simultaneous energy and nitrogen availability may have showed a positive interaction for microorganisms, increasing rumen nitrogen assimilation (Brito et al. 2006; Ramos et al. 2009). Highstreet et al. (2010) reported that high losses of nitrogen in the urine might be due to the fast ruminal hydrolysis of ammoniacal nitrogen. Thus, mesquite pod meal favored protein and energy synchrony, providing a better ruminal microbiota performance and generating a protein with a high biological value without major nitrogen losses (Table 3).

The intake and digestibility of dietary nutrients are interrelated with the existing nitrogen balance in the physiological dynamics of the ruminant animal. Microbial protein keeps the amino acid balance essential to ruminants. Diets were formulated to maintain the same protein levels in the five levels of replacement of corn by mesquite pod meal, with an average value of 121.2 g/kg DM of CP, as well as an average of 544.3 g/kg for TDN (Table 3). Valadares Filho et al. (2010) reported values of 120 g/kg of TDN recommended for cattle growth in Brazilian conditions.

Conclusions

Mesquite pod meal can be used totally replacing corn in Holstein-Zebu crossbred dairy steers’ diet.